Generalist predators, food web complexities and biological pest control in greenhouse crops - Thesis

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Generalist predators, food web complexities and biological pest control in

greenhouse crops

Messelink, G.J.

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2012

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Messelink, G. J. (2012). Generalist predators, food web complexities and biological pest

control in greenhouse crops.

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Generalist predators, food web

complexities and biological pest

control in greenhouse crops

Gerben Messelink

Gerben Messelink

Generalist pr

edators, food web complexities and biological pest contr

ol in gr

eenhouse cr

ops

Generalist predators, food web complexities and

biological pest control in greenhouse crops

G.J. Messelink, 2012. Generalist predators, food web complexities and biological pest control in greenhouse crops

PhD thesis, University of Amsterdam, The Netherlands

Publication of this thesis was financially supported by Koppert Biological Systems (www.koppert.nl)

ISBN: 978 94 91407 04 8

Generalist predators, food web complexities and

biological pest control in greenhouse crops

ACADEMISCH PROEFSCHRIFT

ter verkrijging van de graad van doctor

aan de Universiteit van Amsterdam

op gezag van de Rector Magnificus

prof. dr. D.C. van den Boom

ten overstaan van een door het college voor promoties

ingestelde commissie,

in het openbaar te verdedigen in de Agnietenkapel

op dinsdag 5 juni 2012, te 14:00 uur

door

Gerben Jaap Messelink

geboren te Doornspijk

Promotiecommissie

Promotor:

Prof. dr. M.W. Sabelis

Co-promotor:

Dr. A.R.M. Janssen

Overige leden:

Prof. dr. W. Admiraal Prof. dr. J. Brodeur Prof. dr. T. Hance Prof. dr. S.B.J. Menken Dr. E. Palevsky Dr. P.C.J. van Rijn Dr. M. Venzon

Contents

6 Author addresses

7 1

Introduction

33 2

Evaluation of phytoseiid predators for control of western flower thrips on greenhouse cucumber

47 3

Biological control of thrips and whiteflies by a shared predator: Two pests are better than one

63 4

Positive and negative indirect interactions between prey sharing a predator population

77 5

Pest species diversity enhances control of spider mites and whiteflies by a generalist phytoseiid predator

95 6

Hyperpredation by generalist predatory mites disrupts biological control of aphids by the aphidophagous gall midge Aphidoletes aphidimyza

111 7

Biological control of aphids in the presence of thrips and their enemies 129 8 General discussion 137 Summary 141 Samenvatting 145 Curriculum vitae 145 Publications 147 Dankwoord

Author addresses

Institute for Biodiversity and Ecosystem Dynamics, Section Population Biology, Science Park 904, 1098 XH Amsterdam, The Netherlands

Janssen, Arne van Maanen, Roos Sabelis, Maurice W.

Wageningen UR Greenhouse Horticulture, PO Box 20, 2265 ZG Bleiswijk, The Netherlands

Bloemhard, Chantal M.J. Cortes, Juan A.

van Holstein-Saj, Renata Messelink, Gerben J. Ramakers, Pierre M.J.

Introduction

B

iological control of pest species has traditionally mainly focused on specific nat-ural enemies for each pest (Huffaker & Messenger, 1976; Hokkanen & Pimentel, 1984; van Lenteren & Woets, 1988; Hoy, 1994). However, pest-enemy interactions are often embedded in rich communities of multiple interacting pests and natural enemies (e.g., Helle & Sabelis, 1985b; Minks & Harrewijn, 1989; Sabelis, 1992), and the interactions among these species affect the efficacy of biological control (Sih et al., 1985; Janssen et al., 1998; Prasad & Snyder, 2006; Evans, 2008). The effect of interactions among various species of predators and parasitoids on biological con-trol of a shared pest species has received ample attention (see Letourneau et al., 2009), showing that it can range from larger to smaller than the effect of each enemy species separately (Rosenheim et al., 1995, 1998; Losey & Denno, 1998; Colfer & Rosenheim, 2001; Venzon et al., 2001; Cardinale et al., 2003; Snyder & Ives, 2001, 2003; Finke & Denno, 2004; Cakmak et al., 2009). However, it is not only predator diversity, but also the diversity of herbivorous prey that may affect the suppression of a particular pest species through competition, or indirect interactions mediated by host plant or shared predators (Holt, 1977; Karban & Carey, 1984). Hence, designing effective biological control programs for more than one pest species requires an understanding of all interactions occurring among species within biocontrol commu-nities, not just those among pests and their natural enemies or among different species of natural enemies.

Greenhouse crops are often considered as simple ecosystems with low biodiver-sity (Enkegaard & Brødsgaard, 2006). Especially modern greenhouses appear sterile compared to outdoor crops, as plants are grown on hydroponic systems in green-houses that are isolated from the environment because of modern energy saving techniques (Bakker, 2008). However, the general experience is that infestations by several small pest species cannot be avoided, and the release of natural enemies against these pests adds to the diversity (van Lenteren et al., 2000; Cock et al., 2010). Thus, apparently ‘clean’ greenhouse crops often accommodate complex arti-ficial communities of multiple pests and natural enemies. Furthermore, there seems to be a tendency that the diversity of these communities increased during the last decades (Enkegaard & Brødsgaard, 2006). One reason for this increased diversity is the invasion of exotic pest species (global trade, global warming) (Roques et al., 2009). Second, more species than before develop into pests as a result of the reduced use of pesticides and the use of more selective pesticides (van der Blom et

al., 2009; Pijnakker & Leman, 2011). A third reason is that biological control programs increasingly include generalist predators (Gerson & Weintraub, 2007; Sabelis et al., 2008), and such generalists potentially interfere more with other natural enemies than specialists. Thus, recent developments further increase food web complexity in bio-logical control programs and emphasize that such complexities need to be consid-ered when designing biological control programs. The advantage of greenhouse crops is that they offer the unique possibility to create the desired communities of natural enemies by choosing and releasing natural enemies out of the many species that are commercially available nowadays (van Lenteren, 2000; Enkegaard & Brødsgaard, 2006). In other words, biodiversity can be created and manipulated to maximise sustainable pest control. At the same time, such systems can be used to study the manipulation of biodiversity on the dynamics of communities of plant-inhabiting arthropods under relatively controlled conditions and at larger spatial scales than can usually be realized with communities under field conditions.

Here, I review the ecological theory relevant to interactions in food webs occur-ring within arthropod communities and I discuss the possible implications for biolog-ical control in greenhouses. The subsequent chapters contain studies that focus on the most important greenhouse pests, namely aphids, thrips, spider mites and white-flies, as well as their natural enemies (see BOXESwith pest descriptions).

Food web theory and effects in greenhouse crops

Consumption (i.e., herbivory, predation and parasitism) and competition are consid-ered the two most important interactions determining the structure of communities (Chase et al., 2002). Within communities of natural enemies and pests, species may interact through exploitative competition, through predation and parasitism (includ-ing omnivory, intraguild predation and hyperpredation or hyperparasitism), but also through apparent competition or apparent mutualism via shared natural enemies (FIGURE1.1). Besides these density-mediated interactions, species interactions can be modified through trait changes of the interacting individuals (which includes changes in behaviour and induced plant responses). In the following, I summarize the current theory on these interactions and their relevance to biological control.

Exploitative competition and induced plant responses

Herbivores can interact through exploitative competition for the plant (FIGURE1.1), but this is undesirable for biological control because it occurs at high pest densities, which may exceed the economic damage threshold. I will therefore refrain from dis-cussing resource competition among herbivores here.

Herbivores can also interact via the plant when the attack of one species induces defence responses in the plant that also affect a second species (Karban & Carey,

1984). These plant responses can result in either increased resistance or increased susceptibility (e.g., Karban & Baldwin, 1997; Sarmento et al., 2011a). Plant resistance against insects consists of direct defences, such as the production of toxins and feeding deterrents that reduce survival, fecundity or reduce developmental rate (Kessler & Baldwin, 2002), and indirect defences such as the production of plant volatiles that attract carnivorous enemies of the herbivores (Dicke & Sabelis, 1988; Schaller, 2008). Several biochemical pathways are involved in these processes (Walling, 2000). Recent studies have shown that plant-mediated interactions between herbivores are very common and could be important in structuring herbi-vore communities (Kessler et al., 2007). Models of interactions that are mediated by inducible changes in plant quality predict a range of outcomes including coexistence, multiple equilibria, dependence on initial conditions and competitive exclusion of some herbivore species (Anderson et al., 2009). It should be noted that these mod-els assume that herbivore populations are well mixed and possible variation in induc-tion of plant defences caused by variainduc-tion in populainduc-tion densities is ignored.

Several studies documented indirect interactions between herbivores through induced changes in plant quality (Karban & Baldwin, 1997), but studies on

green-F

FIIGGUURREE11..11 – Schematic diagrams of the direct and indirect interactions among plants, pests and natural enemies that will be treated in this chapter. Arrows indicate consumption. From left to right: exploitative competition in which two pest species compete for the same plant, but also affect each other’s densities through induced plant defences. Apparent competition or apparent mutualism refers to indirect interactions between two prey species mediated by a shared natural enemy (with pests on the same plants this automatically includes exploitative com-petition and induced plant defences). Intraguild predation refers to predators consuming another natural enemy with whom they also compete for the same pest species. Omnivory means consumption on more than one troph-ic level (‘true’ omnivores are predators that feed on both pests and plants). Hyperparasitism or hyperpredation represents the consumption of natural enemies by other natural enemies with whom they do not compete for shared prey, but they differ by the fact that hyperpredators can develop on alternative prey, whereas true hyper-parasitoids are obligate. Except for induced plant responses, these interactions are density mediated.

house crops are limited. In tomato, it has been demonstrated that infestations by caterpillars of a noctuid moth increased resistance to spider mites, aphids and another lepidopteran pest (Stout et al., 1998). Likewise, infestation of tomato and cucumber plants by whiteflies induced resistance against leaf miners (Inbar et al., 1999; Zhang et al., 2005). Induced susceptibility may also occur, for example, infes-tations of tomato plants by whiteflies increased susceptibility to aphids (Nombela et al., 2009). On lima bean, similar results were found for whiteflies and spider mites (Zhang et al., 2009). The spider mite Tetranychus evansi Baker & Pritchard was found to down-regulate plant defences (Sarmento et al., 2011a), and the closely related species Tetranychus urticae Koch can profit from this induced susceptibility (Sarmento et al., 2011b). Induced resistance may also affect the behaviour of omni-vores that facultatively feed on plants. The omnivorous Western flower thrips switched from feeding on cotton plants to feeding on spider mite eggs when defences of the plants were induced (Agrawal et al., 1999). Moreover, they performed worse on a diet of spider mite eggs from induced plants as opposed to non-induced plants (Agrawal & Klein, 2000). In conclusion, plant-mediated interactions among pest species are probably a common phenomenon in greenhouse crops, where they may influence the biological control of multiple pests.

Apparent competition and apparent mutualism

Generalist predators can mediate indirect interactions among prey species that might otherwise not interact (Holt & Lawton, 1994; Janssen et al., 1998; Harmon & Andow, 2004; van Veen et al., 2006) (FIGURE1.1). If, for example, the carrying capac-ity of one prey species increases, this results in an increased equilibrium denscapac-ity of the shared predator and a decreased equilibrium density of the second prey species. Holt (1977) suggested the term ‘apparent competition’ for this interaction between prey species, because the dynamics of the two species resemble that of species competing for resources, whereas in fact it is mediated by the shared predator (see BOXApparent competition). Apparent competition is usually defined as a reciprocal negative interaction between prey species. Most empirical studies, however, show non-reciprocal indirect interactions; only one of the two prey species is negatively affected by the predator-mediated prey interaction (Chaneton & Bonsall, 2000). Originally, the theory of apparent competition considered equilibrium densities. However, generalist predators can also cause ‘short-term’ apparent competition between prey species when predators aggregate in habitat patches containing both prey, or when their feeding rate on one prey is enhanced by the presence of another prey (Holt & Kotler 1987; Müller & Godfray 1997).

The opposite effect may also occur: two prey species that share a natural enemy may also affect each other’s density positively (apparent mutualism). This occurs

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Apparent competition

Apparent competition considers the indirect interaction between two prey species (N1and N2)

that share a predator (P) (Holt, 1977). As an example, I consider two prey species, each with logistic population growth, and a predator population that shows a linear functional response to the densities of the two prey species:

The per capita growth rate is represented by riand the carrying capacity of the prey by Ki. The

per capita predation rate is represented by aiand the per capita population growth rate of the

predators by bi, which can be thought of as a product of the per capita predation rate aiand

the per capita rate of conversion of consumed prey to predators. The per capita mortality rate of the predators is represented by a constant, m. The equilibrium densities can be calculated by setting dNi/dt = 0 and dP/dt = 0. These equilibria have been shown to be stable (Holt, 1977).

For the special case where the predation rate on each of the two prey is equal (a1= a2) and

growth rates of prey and predator are equal (r1= r2; b1= b2), the equilibrium densities are:

This shows that the quilibrium densities of the prey depend on each other’s carrying capac-ity: an increase in the carrying capacity of one prey species (or the addition of a second species to a system of only 1 prey and 1 predator) will decrease the equilibrium density of the other prey species. Such a change is expected when the two prey species compete for the same resource, but this is not the case in the model and therefore their competitive relation must be apparent, i.e., it looks like competition, but results from another mechanism. In fact, as can be seen from the expression for P*, an increase in the carrying capacity of one prey species caus-es an increase the predator equilibrium densiticaus-es and thereby decreascaus-es the equilibrium densi-ty of the other prey species. This can be easily seen from the differential equation of P at equi-librium (dP/dt = 0), which yields P* = 0 or: b1N1* + b2N2* = m. From this it can be seen

direct-ly that an increase in the equilibrium density of one prey species results in a decrease of the density of the other species.

. mP P N b P N b dt dP P N a K N r N dt dN P N a K N r N dt dN 2 2 1 1 2 2 2 2 2 2 2 1 1 1 1 1 1 1 − + = − ⎟⎟⎠ ⎞ ⎜⎜⎝ ⎛ − = − ⎟⎟⎠ ⎞ ⎜⎜⎝ ⎛ − = 1 1

(

)

. * ) ( ) ( * * ⎥ ⎦ ⎤ ⎢ ⎣ ⎡ + − = + = + = 2 1 2 1 2 2 2 1 1 1 K K b m 1 a r P K K b mK N K K b mK N

when increases in the density of one prey species result in satiation of the shared predator. Increases in the density of one prey species can also result in the predator changing from feeding predominantly on a second prey to feeding mainly on the first prey (switching, Murdoch, 1969), consequently reducing the consumption of the sec-ond prey species (Abrams & Matsuda, 1996). This effect is apparent in the short-term, when the densities have not yet reached an equilibrium (transient dynamics), because eventually, the predator populations will increase because of the higher densities of prey, resulting in apparent competition (Abrams & Matsuda, 1996). Apparent mutualism may also occur in the long term when population densities do not reach equilibria, but show cycles, causing repeated satiation of the shared pred-ators and repeated reduced predation on the other prey (Abrams et al., 1998). Hence, depending on the time scale and on the type of dynamics, theory predicts that a shared natural enemy can generate positive or negative indirect effects between prey species.

Apparent competition and apparent mutualism are inherently related to diet choice and switching of the predators from feeding on one prey to feeding on the other prey or on both prey, but effects of mixed diets on predator performance are also relevant. Mixed diets are known to have positive effects on reproduction in some predator species (Wallin et al., 1992; Evans et al., 1999; Toft & Wise, 1999). So far, this aspect of mixed diets has been ignored in theoretical models about apparent competition. Basic models about apparent competition assume that each prey species is suitable for reproduction of the shared natural enemy (Holt, 1977). However, it is also possi-ble that two prey species vary greatly in suitability for the shared natural enemy, for example parasitoids may only marginally develop in some hosts. A model for para-sitoids showed that in such cases, the suitable host can benefit from the presence of the marginal host (assuming no evolution of host preference), but the marginal host suffers from the presence of the suitable host (Heimpel et al., 2003). Observations on aphid parasitoids confirm that unsuitable hosts are indeed attacked by parasitoids in the presence of suitable hosts, which was detrimental for the foraging efficiency of the parasitoid (Meisner et al., 2007).

When generalist predators are released in greenhouse crops, pest species such as thrips, whiteflies, spider mites and aphids can be involved in apparent competi-tion or apparent mutualism. Examples of such generalist predators are anthocorid and mirid bugs and several species of predatory mites. Only few studies on these indirect predator-mediated interactions exist, and they all focused on short-term effects, showing that presence of one pest can release another pest from control (Xu et al., 2006; Desneux & O’Neil, 2008). Although the theory of predator-mediated interactions has long been ignored in many biological control studies, there has been a long-standing interest in the use of alternative prey species for enhancing

biologi-cal control (Stacy, 1977). The method by which these alternative prey species or food are facilitated is based on the introduction of a non-crop plant harbouring the alter-native prey species or providing alteralter-native food sources. It is often referred to as the ‘banker plant method’ (Frank, 2010; Huang et al., 2011). A widely applied system in greenhouse crops is the use of monocotyledonous plants with grain aphids that serve as alternative hosts for parasitoids of aphids that attack the crop (Huang et al., 2011). The elegance of this system is that the grain aphids are host specific and pose no threat to the crop. Plants that produce a lot of pollen may serve as banker plants for generalist predators (Ramakers & Voet, 1995). For example, pollen can serve as food for generalist predatory mites and enhance the biological control of thrips and whiteflies on cucumber (van Rijn et al., 2002; Nomikou et al., 2010). In fact, all kinds of ‘open rearing’ systems of natural enemies in greenhouse crops (e.g., rearing sachets containing small cultures of predatory mites, bran and astigmatic mites) are based on the principles of apparent competition, but there is little awareness that apparent mutualism may also occur.

Intraguild predation

Natural enemies can compete for the same prey species, but this is frequently com-bined with predation by one species of natural enemy on another (Rosenheim et al., 1995), which is called intraguild predation (IGP, FIGURE1.1). The predator that kills and eats the other natural enemy is called the intraguild predator and the other natural enemy is the intraguild prey (Polis et al., 1989; Holt & Polis, 1997).Theory predicts that IGP can only result in stable coexistence of the species when the intraguild prey is the superior competitor for the shared prey, and only in systems with intermediate levels of productivity (Holt & Polis, 1997). These conditions are very restrictive and thus predict that IGP is not common in nature. However, it has become clear that IGP generally occurs in many ecosystems, including biological control systems (Polis et al., 1989; Rosenheim et al., 1995; Janssen et al., 2006, 2007). There may be several reasons for this discrepancy between theory, predicting that systems with strong IGP will be rare, and reality, where IGP is common. Factors that can contribute to the coexistence of intraguild predators and intraguild prey are now increasingly included in theoretical models. Examples of such factors are structured populations with intraguild prey stages that are invulnerable or intraguild predator stages that do not prey on the other predator (Mylius et al., 2001), anti-predator behaviour (Heithaus, 2001), switching intraguild predators (Krivan, 2000) or alternative prey (Daugherty et al., 2007; Holt & Huxel, 2007).

Intraguild predation has been described for many natural enemies that are used for biological control in greenhouse crops (Rosenheim et al. 1995; Janssen et al., 2006). Based on theory, intraguild predation is expected not to benefit biological

con-trol (Rosenheim et al., 1995), but in practice, results are mixed (Janssen et al., 2006, 2007; Vance-Chalcraft et al., 2007). Here, I summarize the occurrence of intraguild predation among natural enemies of thrips, whiteflies, aphids and spider mites. The omnivorous predator Macrolophus pygmaeus (Rambur) (formely identified as Macrolophus caliginosus Wagner) is an intraguild predator of natural enemies of aphids; it consumes the eggs of the syrphid Episyrphus balteatus de Geer (Frechette et al., 2007) and parasitized aphids (Martinou et al., 2009). This predator did not prey on nymphal stages of Orius majusculus (Reuter), but in turn, the nymphal stages of M. pygmaeus were vulnerable for predation by O. majusculus (Jakobsen et al., 2004). Predatory bugs from the genus Orius act as intraguild predators of phytoseiid mites (Gillespie & Quiring, 1992; Venzon et al., 2001; Brødsgaard & Enkegaard, 2005; Chow et al., 2008), the aphidophagous predatory midge Aphidoletes aphidimyza (Rondani) (Hosseini et al., 2010) and aphid parasitoids (Snyder & Ives, 2003). Many generalist predatory mites are intraguild predators of other predatory mites (Schausberger & Walzer, 2001; Montserrat et al., 2008; Buitenhuis et al., 2010; van der Hammen et al., 2010) or juvenile stages of predatory bugs (Madali et al., 2008). Finally, a number of studies show intraguild predation among specialist natural enemies of aphids. The syrphid E. balteatus feeds on freshly parasitized as well as unparasitized aphids (Brodeur & Rosenheim, 2000). Syrphid larvae may also consume the aphidophagous gall midge A. aphidimyza, but predation rates are low in the presence of aphids (Hindayana et al., 2001). In turn, this midge does not prey on E. balteatus (Hindayana et al., 2001), but may consume parasitized aphids (Brodeur & Rosenheim, 2000).

None of the studies mentioned above demonstrate a negative effect of intraguild predation on biological control in greenhouse crops. Although the potential risk of intraguild predation disrupting biological control appears to be low in many cases (Janssen et al., 2006), there are also examples of negative effects of intraguild pre-dation on biological control.

Omnivory

Omnivory in its broadest sense can be defined as the consumption of species at more than one trophic level. Under this definition, intraguild predators are also omni-vores. Predators that feed on both animals and plants are a particular case of troph-ic omnivory, also referred to as ‘true omnivory’ (Coll & Guershon, 2002). The first the-oretical models on its dynamical consequences showed that omnivory destabilizes food webs (Pimm & Lawton, 1978), which is remarkable, considering the fact that omnivory is a common interaction in food webs (Coll & Guershon, 2002; Polis & Strong, 1996). More specific theory for plant-feeding omnivores shows that omni-vores can stabilize the dynamics and persistence of populations by switching between consuming plants and prey, especially when the searching efficiency of the

predator for prey is low relative to that for plant tissue (Lalonde et al., 1999). Hence, this theory suggests that biological control with plant-feeding omnivores may stabi-lize pest population dynamics. The question is, whether these equilibrium densities are acceptable for pest control (Lalonde et al., 1999). Other aspects of plant-feeding omnivory, such as the persistence of predators in the absence of prey, or the nutri-tional benefits for predators of feeding on plants may also result in positive contribu-tions to biological control.

Many predators that are used for biological control are true omnivores, feeding on pests and plant-provided food such as pollen, nectar and plant saps. For

exam-BOX

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Thrips

Western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), is one of the most important pest species in greenhouse crops in Europe and North America (Lewis, 1997; Shipp & Ramakers, 2004). Damage of plants results from both feed-ing on leaves, flowers and fruits, as well as by transmission of virus-es. Although F. occidentalis is primarily considered a phytophagous

species that feeds on plant tissue, plant nectar or pollen, it is actually an omnivore. The larvae and adults facultatively feed on spider mite eggs (Trichilo & Leigh, 1986), on predatory mite eggs (Faraji et al., 2001; Janssen et al., 2003), or on whitefly crawlers (van Maanen et al., in press). Biological control of Western flower thrips in greenhouses started with mass releases of the phytoseiid predatory mite Neoseiulus barkeri (Hughes) (= Amblyseius mckenziei) (Ramakers, 1980). Phytoseiid mites are still the most important thrips predators in many greenhouse crops nowadays (Gerson & Weintraub, 2007). Most of them are omnivorous; they do not only feed on thrips, but also on other prey, as well as and plant provided food such as pollen (for overviews see McMurtry & Croft, 1997; Gerson & Weintraub, 2007). A second important group of thrips predators are anthocorid bugs. The species most used in Europe is Orius laevigatus (Fieber), in Northern America it is Orius insidiosus (Reuter) (Brødsgaard, 2004; Shipp & Ramakers, 2004). These predators are released especially in (sweet) pepper crops where the continuous presence of pollinating flowers supplies sufficient food for establishment of predator populations even when prey is scarce (van den Meiracker & Ramakers, 1991). Although anthocorid bugs are mainly released for thrips control, they can also contribute to the control of whiteflies (Arnó et al., 2008), aphids (Alvarado et al., 1997; Butler & O'Neil, 2007), Lepidoptera species (Jacobson & Kring, 1994) and spider mites (Janssen et al., 1998; Venzon et al., 2002). Finally, thrips are sometimes controlled through releases of soil-dwelling predatory mites of the family of Laelapidae or Macrochelidae, which feed on the pupae of thrips in the soil (Gillespie & Quiring, 1990; Berndt et al., 2004; Messelink & van Holstein, 2008).

ple, many generalist predatory mites and bugs can complete their life cycle when feeding on pollen. However, not all greenhouse crops produce edible pollen, but some omnivores, such as the mirid bug M. pygmaeus, can also live and reproduce on plant saps. Although considered as a pest species, Western flower thrips, Frankliniella occidentalis (Pergande) are in fact omnivorous predators that feed on spider mites, predatory mites, whiteflies and plants (Trichilo & Leigh, 1986; Faraji et al., 2001; Janssen et al., 2003; van Maanen et al., in press). The consumption of prey in addition to plant material by mirid bugs and thrips can increase reproduc-tion and developmental rates of these omnivores (Janssen et al., 2003; Perdikis & Lykouressis, 2004). The quality of the host plant can affect the predation rates of omnivores on pests (Agrawal et al., 1999; Agrawal & Klein, 2000; Magalhães et al., 2005; Hatherly et al., 2009) or the extent to which intraguild predation occurs (Janssen et al., 2003; Shakiya et al., 2009). Thus for biological control with preda-tors that can also feed on the plant, it is important to known that the dynamics will be affected by plant quality.

Hyperpredation and hyperparasitism

In contrast to intraguild predation, natural enemies can also be consumed by other predators or parasitoids without sharing a prey with these enemies. Thus there is no competition for prey between the natural enemies. In parasitoids, the dynamical con-sequences of this so-called hyperparasitism are well-studied, both theoretically (Beddington & Hammond, 1977; May & Hassell, 1981) and empirically (Sullivan & Völkl, 1999). These studies indicate that obligate hyperparsitoids (secondary para-sitoids that can develop only in or on a primary parasitoid) always lead to an increase of the pest equilibria, which might be detrimental to biological control. In case the hyperpredator is a true predator, there is no agreement in the literature on the name of this type of interaction. Some prefer to use the term ‘secondary predation’ (Rosenheim et al., 1995), or ‘higher-order predation’ (Rosenheim, 1998; Symondson, 2002) for predators consuming other predators, which includes both hyperpredation and intraguild predation. Even more confusing is that some interactions are described as hyperpredation, whereas it would be more consistent to typify them as apparent competition (e.g., Courchamp et al., 2000; Roemer et al., 2001) or intraguild predation (e.g., Roemer et al., 2002). In this thesis, I suggest to use the term hyper-predation in cases where predators eat other predators without sharing a prey, because of its similarity to hyperparasitism. However, an important difference is that hyperpredators can develop on alternative prey or food, whereas most hyperpara-sitoids specifically reproduce on or in other parahyperpara-sitoids. In the presence of alterna-tive prey, hyperpredation can be classified as apparent competition between the alternative prey and the specialist natural enemy. To my knowledge, no specific

the-ory has been formulated on the effects of hyperpredation on prey populations in the presence of alternative prey. Theory on apparent competition predicts that the pres-ence of one prey lowers the equilibrium densities of the second prey. For hyperpre-dation, this would mean that increases in the densities of the alternative prey will results in lower equilibrium densities of the specialist natural enemy, which would consequently release the prey of the specialist from control. In the short-term, satia-tion effects of the hyperpredator might result in apparent mutualism between the alternative prey and the specialist natural enemy. Hence, there will be a reduced neg-ative effect on pest control by the specialist natural enemy.

In greenhouse crops, predatory mites that are used for control of thrips have been observed to be hyperpredators. They feed on eggs of predatory midges, but not on aphids, the pest that is controlled by larvae of predatory midges (van Schelt & Mulder, 2000). The impact of this type of interaction will receive more attention in this

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Whiteflies

Whiteflies are among the most important pest species of agricultural crops world wide. The species that cause damage to greenhouse crops are the polyphagous tobacco whitefly Bemisia tabaci Gennadius and the greenhouse whitefly Trialeurodes vaporariorum (Westwood). In Northern European greenhouses, the dominant species is the greenhouse whitefly, which was the reason to use this

species in this thesis. Whitefly damage is caused by nymphs and adults feeding on phloem, but also through the honeydew produced by the feeding stages, which contaminates the leaves. This facilitates the growth of sooty mold, which reduces photosynthesis (Byrne & Bellows, 1991). Biological control of T. vaporariorum in greenhouses started in the UK with the parasitoid Encarsia formosa Gahan (Speyer, 1927) and this wasp is still one of the biggest suc-cess stories in greenhouse biological control (van Lenteren, 2000). Since then, many other arthropods have been described as natural enemies of whiteflies, but only few species are applied commercially (Gerling et al., 2001). The most important species in greenhouse crops are the parasitoids E. formosa, Eretmocerus mundus Mercet and Er. eremicus Rose & Zol-nerowich, the mirid bug Macrolophus pygmaeus (Rambur) (formely identified as Macrolophus caliginosus Wagner) and the predatory mite Amblyseius swirskii Athias-Henriot (Nomikou et al., 2002; Cock et al., 2010). The generalist predator M. pygmaeus is released mainly to con-trol whiteflies (Gerling et al., 2001), although it has been observed to contribute to the concon-trol of aphids (Alvarado et al., 1997; Fantinou et al., 2009), thrips (Riudavets & Castañé, 1998; Blaeser et al., 2004), spider mites (Hansen et al., 1999), leaf miners (Arnó et al., 2003) and Lepidoptera species (Urbeja et al., 2009).

thesis. Hyperparasitism is common in the biological control of aphids in greenhous-es and can disrupt biological control (Mgreenhous-esselink, personal observations).

Effect of flexible behaviour

The interactions occurring in food webs that were described above all concern den-sity-mediated interactions among species. However, it is generally recognized that traits of individuals, such as behaviour or defence, can change in response to the presence of individuals of other species (so-called trait-mediated interactions, Werner & Peacor, 2003). For example, anti-predator behaviour can strengthen or weaken density-mediated effects (Prasad & Snyder, 2006; Janssen et al., 2007). Many of these behavioural changes are mediated by chemical cues, which are released or left behind by both natural enemies and prey (Dicke & Grostal, 2001). Theoretical models of community dynamics now increasingly try to study the conse-quences of these behavioural-mediated interactions (e.g., Holt & Kotler, 1987; Abrams, 2008). These models show that the effects of such interactions may change the dynamics of the interacting species substantially.

Many interactions among natural enemies and pests in greenhouses can be affected by changes in the behaviour of pest and natural enemy. First of all, it is known that pest species can avoid their enemies. For example, whiteflies can learn to avoid plants with generalist predatory mites (Nomikou et al., 2003) and spider mites avoid plants with the predator Phytoseiulus persimilis Athias-Henriot (Pallini et al., 1999) or with thrips, which is a competitor and intraguild predator (Pallini et al., 1997). Aphids are well-known for their antipredator responses. For example, they kick at natural enemies, or they walk away or drop off the plants when perceiv-ing a natural enemy (Villagra et al., 2002). Aphids as well as thrips release alarm pheromones that alert conspecifics (Bowers et al., 1972; Teerling et al., 1993; de Bruijn et al., 2006). Thrips can avoid predation by predatory bugs and predatory mites by using spider mite webbing as a refuge (Pallini et al., 1998; Venzon et al., 2000). They can defend themselves against predators by swinging with their abdomen and producing defensive droplets (Bakker & Sabelis, 1989), or even by counter-attacking the vulnerable egg stages of their phytoseiid predators (Faraji et al., 2001; Janssen et al., 2002). Natural enemies also respond to threats of other (intraguild) predators or counter-attacking prey. Predatory mites avoid ovipositing near counter-attacking thrips (Faraji et al., 2001) or intraguild predators (Choh et al., 2010; van der Hammen et al., 2010), or retain eggs in the presence of intraguild predators (Montserrat et al., 2007). Aphid parasitoids are known to avoid intraguild predation once they detect the chemical cues of the intraguild predators (Nakashima et al., 2006). The effects of intraguild predation can also be changed by the prey preference of the intraguild predator. For example, the syrphid E.

baltea-tus is an intraguild predator of aphid parasitoids because it consumes parasitized aphids, but when given a choice, it prefers to oviposit in aphid colonies without par-asitized aphids (Pineda et al., 2007), thus weakening the effects of intraguild pre-dation.

Interactions among species may change over time through learning or experi-ence (Nomikou et al., 2003). For example, the predatory bug O. majusculus was more successful at preying on aphids after learning how to avoid the prey’s kicking response (Henaut et al., 2000). Furthermore, predation rates on a specific pest might change through the presence of alternative food: the predatory bug O. laevi-gatus increased the predation rates on thrips in the presence of pollen (Hulshof & Linnamäki, 2002). Thus somehow, the pollen seemed to stimulate the feeding behaviour of these predators. In contrast, the presence of unsuitable prey may reduce the efficacy of a natural enemy for the target pest. For example, studies with parasitoids demonstrated that spending foraging time or eggs on less-suitable hosts will decrease parasitoid foraging success and ultimately decrease parasitoid population size (Meisner et al., 2007). Such effects may also occur in greenhouses when mixtures of aphid species are present in a crop. The reason why parasitoids attack unsuitable or marginal hosts in the study by Meisner et al. (2007) is not clear, perhaps the parasitoids and marginal hosts have not coevolved and there has been no selection on the parasitoid to discriminate between the marginal host and other host species. The examples presented above show that multiple prey effects can

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Spider mites

The most important spider mite pest in greenhouse crops is the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) (Gillespie & Raworth, 2004). This polyphagous pest causes damage to plants by puncturing the plant cells and feeding on their contents (Helle & Sabelis, 1985a). Moreover, they produce protective silk webs (Sabelis & Bakker, 1992), which eventually can completely cover

infested plants. Biological control of spider mites with the specialist predatory mite Phytosei-ulus persimilis Athias-Henriot is one of the cornerstones of biological control in greenhouse crops (Bravenboer & Dosse, 1962; Hussey & Bravenboer, 1971). Many other commercially applied phytoseiid predators feed on spider mites, but they are less specialized and feed on other prey as well (McMurtry & Croft, 1997). Other generalist predators, mentioned above, may also contribute to the suppression of spider mites in greenhouse cops, but most of them are hindered by the dense web produced by the spider mites (Sabelis & Bakker, 1992).

change the behaviour of shared natural enemies and may determine the outcomes of biological control.

Summarizing, changes in interactions or interaction strengths through flexible behaviour are common among the pests and natural enemies in greenhouse crops. Thus, when designing and interpreting results of multi-species experiments, it should be realized that both density-mediated interactions and behaviour-mediated interac-tions affect biological control.

Conclusions food web theory

Food web theory can provide insight into how various interactions between species might affect species dynamics and their possible effects on biological control. However, since models are based on simplifying assumptions, theoretical predic-tions are bound to differ from empirical studies (e.g., Janssen et al., 2006; Rosenheim & Harmon, 2006). One important reason for this is that theory is often tailored to predict equilibrium dynamics, whereas biological control systems often concern short-term (transient) dynamics, which might differ from long-term dynam-ics (Bolker et al., 2003; Briggs & Borer, 2005). A second reason is that food webs in reality are much more complex than theoretical models assume (Rosenheim et al., 1995; May, 1999; Coll & Guershon, 2002; Bolker et al., 2003; Cardinale et al., 2003; Janssen et al., 2006, 2007; Letourneau et al., 2009). The presence of multiple pests and natural enemies will result in joint effects of several types of interactions, and there is limited theory that takes such complexity into account. Furthermore, most models assume that populations are well mixed, whereas in reality arthropod pop-ulations are often clustered either within plants or within crops. To close these gaps between theory and practice, more long-term experiments are needed to observe dynamics of natural enemies and pest species over a sufficient number of genera-tions to allow reaching equilibria. Furthermore, experimental studies in which food web complexity is varied systematically are needed to test the relative importance of theoretical predictions. Greenhouse crops are ideally suited for this latter type of studies, because artificially created communities in biocontrol systems can be manipulated easily. Similarly, greenhouse experiments could give insight into short-term dynamics of interactions for which only equilibrium theory is available. The diversity and complexity of some artificial food webs in greenhouse vegetable crops is presented in the next section.

Food webs in greenhouse crops

The complexities of arthropod communities associated with biocontrol systems varies among crops, because crops differ in susceptibility to pests species and suit-ability for natural enemies. Here, I present examples of food webs and their

interac-tions in cucumber and sweet pepper, the two crop systems studied in this thesis. The most important pests in greenhouse cucumber in Europe and North America are thrips, whiteflies, spider mites and cotton aphids (Shipp, 2004). Modern varieties of greenhouse cucumber are parthenocarpic, so do not produce pollen. This is the reason for generalist predatory bugs not performing well in this crop. The natural enemies used in cucumber are mainly specialized whitefly parasitoids, aphid para-sitoids and predatory midges and some specialist and generalist predatory mites (FIGURE1.2). The interactions in food webs presented in FIGURE1.2 are based on the literature review presented above.

The second example concerns greenhouse sweet pepper. This is one of the crops where the release of natural enemies for biological control has resulted a complex system of multiple pests and natural enemies, including several different species of generalist predators. These generalists establish easily in this crop, because the plants flower continuously and thus supply nectar and pollen as food for the

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Aphids

Almost every greenhouse crop is attacked by one or more species of aphids. The green peach aphid, Myzus persicae (Sulzer) is the most common species, attacking a wide range of host plants. In this the-sis, I used a red phenotype of M. persicae, which causes serious damage in sweet pepper (Gillespie et al., 2009). Other important aphids in greenhouse crops are the foxglove aphid Aulacorthum

solani (Kaltenbach) and the cotton aphid Aphis gossypii Glover (Ramakers, 1980; Blümel, 2004). Aphids are phloem feeders and weaken plants by draining their resources and causing severe distortion of growth. Moreover, aphids produce large amounts of honeydew, which can completely cover leaves. This facilitates the growth of sooty mold, which consequently reduces photosynthesis. Aphids reproduce extremely fast (Wyatt & Brown, 1977), which can result in rapid destruction of the crop. Biological control of aphids in greenhouse crops is cur-rently mainly based on releases of the parasitoids Aphidius colemani Viereck, Aphidius ervi Haliday, Aphelinus abdominalis Dalman and the aphidophagous gall midge Aphidoletes aphidimyza (Rondani) (Cock et al., 2010, Table 4). Less commonly applied are syrphids, Episyrphus balteatus de Geer and chrysopids of the Chrysoperla carnea-group, whose larvae are rather specialized aphid predators. The experience is, however, that these predators hard-ly establish in greenhouse crops as the adults tend to fhard-ly away (Ramakers, 1980). Coccinellids are generally recognized as important aphid predators, but hardly used in greenhouses because they also escape. Finally, aphid control may partly be based on generalist predatory bugs which feed on multiple prey, as discussed above.

tors. The most important pests in sweet pepper crops in greenhouses in temperate regions are thrips, spider mites and aphids (Ramakers, 2004), whereas in Mediterranean countries, one of the major pest species is the tobacco whitefly (Calvo et al., 2009). Many other pest species can attack sweet pepper, such as caterpillars of noctuid moths, broad mites, leaf miners and mirid bugs, but they are less impor-tant than the pests mentioned above (Ramakers, 2004). Nevertheless, the simultane-ous occurrence and need to control these latter pests species results in a complex food web of interacting species (FIGURE1.3).

The food webs presented in FIGURE1.2 and 1.3 show that the interactions between a certain pest and its natural enemies are often embedded in a complex web of inter-actions. For example, intraguild predation is often accompanied by apparent compe-tition between the intraguild prey and several other alternative prey species. Furthermore, the intraguild predators or hyperpredators can also feed on plant-pro-vided food, with the result that plant quality may affect intraguild predation or

hyper-F

FIIGGUURREE11..22 – A food web of pest species and their most commonly used natural enemies in cucumber. Arrows indicate consumption. Generalist predators are phytoseiid predatory mites (g). Specialist enemies of aphids are parasitoids from the genus Aphidius (A. sp.) and the predatory midge Aphidoletes aphidimyza (A. a.). Parasitoids are commonly attacked by several species of hyperparasitoids (h). The specialist predator of spider mites is

Phytoseiulus persimilis (P. p.). Specialist parasitoids of whiteflies are wasps from the genus Eretmocerus, or Encarsia formosa (E. sp.).

predation (Agrawal & Klein, 2000; Janssen et al., 2003). This illustrates the complex-ity of biological control, where effects of some interactions may override the effects other interactions (Polis & Strong, 1996). Thus, the study of particular species inter-actions, such as those between a pest and its natural enemy, should be embedded in empirical studies and models that capture the essence of realistic food webs. Although it may be difficult to disentangle all possible interactions and their impor-tance for biological control, the understanding of such interactions will help in design-ing effective communities of natural enemies for the suppression of multiple pests. Furthermore, although complex, the artificial food webs of biological control systems are less intricate than most natural systems, and the manipulation of species densi-ties in biological control systems is easier than in natural food webs. Biological con-trol systems therefore offer ideal opportunities for testing food web theory.

F

FIIGGUURREE11..33 – A food web of pest species and their most commonly used natural enemies in sweet pepper crops. Arrows indicate consumption. The generalist predators are bugs from the genus Orius (O. sp.), the mirid bug

Macrolophus pygmaeus (M. p.) and generalist phytoseiid predatory mites (g). Specialist enemies of aphids are

parasitoids from the genus Aphidius (A. sp.), the predatory midge Aphidoletes aphidimyza (A. a.) and the syrphid

Episyrphus balteatus (E. b.). Parasitoids are commonly attacked by several species of hyperparasitoids (h). The

specialist predator of spider mites is Phytoseiulus persimilis (P. p.). The main whitefly species in sweet pepper is

Outline of this thesis

In this thesis, I study several types of interactions in food webs that occur within arthropod communities on greenhouse crops subject to biological pest control with generalist predators. The central question in all these studies is to which extent pat-terns expected from food web theory can be identified from the dynamics of arthro-pod communities in greenhouse crops when using generalist predators, and how interactions in food webs affect the suppression of pest species. In the first part of this thesis, I describe the selection and evaluation of generalist predatory mites for control of thrips and whiteflies in greenhouse cucumbers, and how these predators mediate indirect interactions such as apparent competition and apparent mutualism among thrips, whiteflies and spider mites. In the second part of the thesis, I study the conflicting interactions among predators that are used for biological control of aphids and thrips in sweet pepper, with special emphasis on hyperpredation. In this case, apparent competition occurs between a pest and a natural enemy of another pest. The interactions I studied may serve as tests of general theories on commu-nity ecology and contribute to better strategies for multiple pest control in green-house crops.

The work described in this thesis started with the selection and evaluation of gen-eralist predators for multiple pest control. I tested several species of predatory mites for the control of thrips in cucumber (CHAPTER2). The finding of generalist predatory mites that are able to control both thrips and whiteflies gave rise to the question how pest control with a generalist predator works when the two pest species are present simultaneously. In such a case, the two pest species are involved in apparent com-petition, and, as outlined above, this may have positive or negative effects on the pest densities. In CHAPTER3, I present the population dynamics of thrips and white-flies in the presence of their shared predators Amblyseius swirskii or Euseius ovalis. The indirect predator-mediated interactions between thrips and whiteflies are further studied in CHAPTER4, where I manipulated the dynamics of whiteflies in such a way, that it would result in positive effects on thrips densities through a shared predator (so-called apparent mutualism). In CHAPTER5, I increased the food web complexity in cucumber by adding spider mites as a third pest species to the system of thrips, whiteflies and the generalist predator A. swirskii. In greenhouse trials, I study the effects of A. swirskii on spider mites in the presence and absence of other pest species. In CHAPTER6, I demonstrate how generalist predatory mites may affect the control of aphids by feeding on the important aphid predator, the gall midge A.

aphidimyza. CHAPTER 7 shows the effects of generalist predators on the control of

aphids and thrips in sweet pepper. Specialist aphid parasitoids and predatory midges were released together with either N. cucumeris, a predator of thrips and a hyperpredator of the predatory midge, or Orius majusculus (Reuter), a predator of

thrips and aphids and intraguild predator of both specialist natural enemies. In CHAPTER8, I highlight the most important findings of this thesis, discuss these in a broader context of biological control and food web theory and give some ideas and directions for future research.

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